Molecular Systematics of New World Suboscine Birds R

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Available online at www.sciencedirect.com MOLECULAR SCIENCEENCE^I /W) DIRECT® PHYLOGENETICS AND EVOLUTION ELSEVIER Molecular Phylogenetics and Evolution 32 (2004) 11-24 www.elsevier.com/locate/ympev

Molecular systematics of New World suboscine birds R. Terry Chesser*

Department of Ornithology, American Museum of Natural History, Central Park West at 79 th Street, New York, NY 10024, USA Received 12 February 2003; revised 14 November 2003 Available online 4 February 2004

Abstract

Pliylogenetic relationships among New World suboscine birds were studied using nuclear and mitochondria! DNA sequences. New World suboscines were shown to constitute two distinct lineages, one apparently consisting of the single species Sapayoa aenigma, the other made up of the remaining 1000+ species of New World suboscines. With the exception oí Sapayoa, monophyly of New World suboscines was strongly corroborated, and monophyly within New World suboscines of a tyrannoid clade and a furnarioid clade was likewise strongly supported. Relationships among families and subfamilies within these clades, however, differed in several respects from current classifications of suboscines. Noteworthy results included: (1) monophyly of the tyrant- flycatchers (traditional family Tyrannidae), but only if the tityrines (see below) are excluded; (2) monophyly of the pipromorphine flycatchers (Pipromorphinae of Sibley and Ahlquist, 1990) as one of two primary divisions of a monophyletic restricted Tyrannidae; (3) monophyly of the tityrines, consisting of the genus Tityra plus all sampled species of the Schiffornis group (Prum and Lanyon, 1989), as sister group to the manakins (traditional family Pipridae); (4) paraphyly of the ovenbirds (traditional family Furnariidae), if woodcreepers (traditional family Dendrocolaptidae) are excluded; and (5) polyphyly of the antbirds (traditional family Formi- cariidae) and paraphyly of the ground antbirds (Formicariidae sensu stricto). Genus Melanopareia (the crescent-chests), although clearly furnarioid, was found to be distant from other furnarioids and of uncertain aflSnities within the Furnarii. Likewise, the species Oxyruncus cristatus (the Sharpbill), although clearly tyrannoid, was distantly related to other tyrannoids and of uncertain aflSnities within the Tyranni. Results of this study provide support for some of the more novel features of the suboscine phylogeny of Sibley and Ahlquist (1985, 1990), but also reveal key differences, especially regarding relationships among suboscine families and subfamilies. The results of this study have potentially important imphcations for the reconstruction of character evolution in the suboscines, especially because the behavioral evolution of many suboscine groups (e.g., Furnariidae) is of great interest. © 2003 Elsevier Inc. All rights reserved.

1. Introduction sively in the tropics of the Old World, where they appear to be relictually distributed (Mayr and Amadon, 1951). Suboscine, or non-oscine, birds are one of two major Although suboscines were defined in part based on components of tlie large avian order Passeriformes lack of a character•they are passerine birds that lack (passerines) and consist of roughly 1150 species, or the oscine, or songbird, syrinx•and have been referred about one-eighth of extant birds. Found throughout the to as "this by no means natural group" (Stresemann, Americas, they account for more than 30% of the 1934, translated in Sibley, 1970), the modern view is that world's richest avifauna, that of the Neotropics, where suboscines are monophyletic relative to other passerines they have undergone a remarkable large-scale radiation. and that they consist of two monophyletic groups Suboscines are predominantly a New World group, but divisible along geographical lines: the New World su- the 51 species of the families Eurylaimidae (broadbills), boscines and the Old World suboscines (Irestedt et al., Philepittidae (asities), and Pittidae (pittas) occur exclu- 2001; Raikow, 1987; Raikow and Bledsoe, 2000; Sibley and Ahlquist, 1990). New World suboscines are likewise generally con- Present address: Australian National Wildlife Collection, CSIRO Sustainable Ecosystems, GPO Box 284, Canberra ACT 2601, Austra- sidered to consist of two monophyletic groups, one lia. Fax: 1-61-2-6242-1688. ("Tyranni" in Ames, 1971 and Raikow, 1987, "Tyr- E-mail address: [email protected]. annida" in Sibley and Ahlquist, 1990) consisting of the

1055-7903/$ - see front matter © 2003 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2003.11.015 12 R T. Chesser I Molecular Phylogenetics and Evolution 32 (2004) 11-24 tyrant-flycatchers and relatives, the other ("Furnarii" of New World suboscines, and (3) the relationships of in Ames, 1971 and Raikow, 1987, "Furnariida" and suboscine taxa of uncertain affinities. "Thamnophilida" in Sibley and Ahlquist, 1990) consisting of the ovenbirds, antbirds, and related taxa. The Tyranni contain many taxa of uncertain familial affini- 2. Materials and methods ties, variously placed in the traditional families Tyran- nidae (tyrant-flycatchers), Pipridae (manakins), or Fifty-three taxa were sampled (Table 1), including Cotingidae (cotingas), including members of the Schif- one non-passerine (the woodpecker Campethera nivosa), fornis group (Prum and Lanyon, 1989) and the Sharpbill four oscine passerines (two representatives of each os- Oxyruncus cristatus. Species composition of families in cine parvorder in Sibley and Ahlquist, 1990), one pas- the Furnarii (sensu Ames, 1971 and Raikow, 1987), in serine of uncertain affinities (the New Zealand wren contrast, has with few exceptions been well defined, but Acanthisitta chloris), three Old World suboscines (one the monophyly and relationships of specific families representative from each family), and 44 New World have been a matter of debate. suboscines. Taxon sampling among New World subos- Although most previous systematic work on suboscines was guided largely by the phylogeny of Sibley and cines has been based on morphology, Sibley and Ahl- Ahlquist (1985, 1990) and the classification of Sibley and quist (1985, 1990) produced a detailed phylogenetic Monroe (1990), and was designed to establish relation- hypothesis of New World suboscines based on DNA- ships among major groups, to provide simple tests of the DNA hybridization data (Fig. 1). This phylogeny was monophyly of major groups, and to indicate relation- consistent in some ways with traditional classifications, ships of problematical taxa. The following were con- but it contained several striking features, including sidered major groups for sampling purposes, using the polyphyly of the traditional family Tyrannidae (species nomenclature of Sibley and Monroe (1990), with num- included in the Tyranninae and Pipromorphinae of ber of taxa sampled in parentheses: Pipromorphinae (5), Sibley and Ahlquist) and polyphyly of the traditional Tyranninae (4), Tityrinae (3), Cotinginae (5), Piprinae family Formicariidae (species included in the Formi- (3), Furnariinae (6), Dendrocolaptinae (3), Thamno- cariidae and Thamnophilidae of Sibley and Ahlquist). philidae (4), Formicariidae (4), Conopophagidae (2), Polyphyly of the traditional Formicariidae has also been and Rhinocryptidae (4). The Broad-billed Sapayoa, supported by a recent study using DNA sequence data Sapayoa aenigma, a New World suboscine of uncertain (Irestedt et al., 2002). affinities, was also sampled. Larger numbers of taxa Below I provide a phylogenetic hypothesis for New were sampled for groups with relatively large numbers World suboscines based on DNA sequence data, and of species (e.g., Furnariidae) or for more controversial use this hypothesis to address: (1) the monophyly of groups (e.g., Pipromorphinae), and smaller numbers for New World suboscines, (2) the monophyly and relatively small groups (e.g., Conopophagidae). Taxa relationships of traditional and non-traditional groups within major groups were chosen to be as divergent as possible, to strengthen tests of monophyly and to break OW suboscines up long branches for phylogenetic analysis. Intron 7 of the nuclear gene ß-fibrinogen and the Tyranninae complete mitochondrial genes ND3 and COII were se- Tityrinae quenced for all taxa, with two exceptions. Complete mitochondrial but only partial ß-fibrinogen sequence Cotinginae was obtained for Melanopareia torquata, and complete ß-fibrinogen but no mitochondrial sequence was ob- Piprinae tained for A. chloris. Tissue samples were collected Pipromorpliinae during fieldwork in South America and from the De- partment of Ornithology, American Museum of Natural Furnariidae History, New York, NY; the Genetic Resources Col- lection, Louisiana State University Museum of Natural Formicariidae Science, Baton Rouge, LA; the Division of Birds, Field Museum of Natural History, Chicago, IL; the Royal Rliinocryptidae Ontario Museum, Toronto, Ont.; the Marjorie Barrick Conopophagidae Museum, University of Nevada Las Vegas, Las Vegas, NV; and the University of Arizona Bird Collection, Thamnoplniiidae Tucson, AZ. Sequences were obtained using DNA ex- Fig. 1. Phylogenetic hypothesis of suboscine birds based on DNA- tracted from tissue by means of a 5% Chelex solution DNA hybridization data (Sibley and Ahlquist, 1985, 1990). This is (Walsh et al., 1991). Primers used for initial PCR Sibley and Ahlquist's preferred tree, obtained using UPGMA analysis. amplification of intron 7 were FIBI7U and FIBI7L, both R. T. Chesser I Molecular Phylogenetics and Evolution 32 (2004) 11-24 13

Table 1 List of species name, tissue reference number, and putative taxonomic affinities of sequenced individuals Species Tissue number Higher group Family (prior to Sibley Family/Subfamily and Monroe) (Sibley and Monroe) Mionectes okaginea AMNH GFB 2231 Tyranni Tyrannidae Pipromorphinae Leptopogon amaurocephalus AMNH RTC 312 Tyranni Tyrannidae Pipromorphinae Hemitriccus MBM GAV 1001 Tyranni Tyrannidae Pipromorphinae margaritaceiven ter Todirostrum cinereum AMNH PEP 2051 Tyranni Tyrannidae Pipromorphinae Corythopis torquata AMNH PEP 2014 Tyranni Tyrann./Conopo. Pipromorphinae Muscisaxicola capistrata AMNH RTC 377 Tyranni Tyrannidae Tyranninae Elaenia alhiceps AMNHPRS 1136 Tyranni Tyrannidae Tyranninae Tyrannus melancholicus AMNH PRS 1090 Tyranni Tyrannidae Tyranninae Laniocera hypopyrra AMNH GFB 1401 Tyranni Piprid./Cot./Tyrann. Tyranninae Tityra semifasciata AMNH GFB 1035 Tyranni Coting./Tyrann. Tityrinae Pachyramphus marginatus AMNH GFB 1407 Tyranni Coting./Tyrann. Tityrinae Schijfornis turdinus AMNH GFB 2223 Tyranni Piprid./Cot./Tyrann. Tityrinae lodopleura isahellae LSU B-4184 Tyranni Coting./Tyrann. Cotinginae Procnias alba AMNH ROP 309 Tyranni Cotingidae Cotinginae Rupicola rupicola AMNH PEP 1962 Tyranni Cotingidae Cotinginae Phytotoma rutila AMNHPRS 1153 Tyranni Phytotom./Coting. Cotinginae Oxyruncus cristata LSU B-2186 Tyranni Oxyrun./Tyrann./Cot. Cotinginae Pipra pipra AMNH GFB 2080 Tyranni Pipridae Piprinae Machaeropterus deliciosus FMNH 11761 Tyranni Pipridae Piprinae Tyranneutes stolzmanni AMNH CJW 104 Tyranni Pipridae Piprinae Sapayoa aenigma LSU B-2330 Tyranni Piprid./Tyrann. (incertae sedis) Geositta cunicularia AMNH APC 3280 Furnarii Furnariidae Furnariinae Margarornis ruhiginosus AMNH GFB 1024 Furnarii Furnariidae Furnariinae Furnarius rufus AMNH RTC 389 Furnarii Furnariidae Furnariinae Synallaxis cinerascens AMNH RTC 326 Furnarii Furnariidae Furnariinae Automolus rufipileatus AMNH GFB 2079 Furnarii Furnariidae Furnariinae Sclerurus mexicanus AMNH ROP 108 Furnarii Furnariidae Furnariinae Lepidocolaptes fuscus AMNH APC 96-11 Furnarii Dendrocolaptidae Dendrocolaptinae Dendrocincla fuliginosa AMNH SC 771 Furnarii Dendrocolaptidae Dendrocolaptinae Drymornis hridgesii LSU B-25799 Furnarii Dendrocolaptidae Dendrocolaptinae Frederickena viridis AMNH ROP 281 Furnarii Formicariidae Thamnophilidae Myrmotherula haematonota AMNH GFB 2189 Furnarii Formicariidae Thamnophilidae Pithys alhifrons AMNH GFB 2078 Furnarii Formicariidae Thamnophilidae Pyriglena leucoptera AMNH RTC 317 Furnarii Formicariidae Thamnophilidae Formicarius colma AMNH SC 721 Furnarii Formicariidae Formicariidae Grallaria ruficapilla AMNH GFB 3159 Furnarii Formicariidae Formicariidae Grallaricula nana AMNH ROP 362 Furnarii Formicariidae Formicariidae Myrmothera simplex AMNH GFB 2136 Furnarii Formicariidae Formicariidae Conopophaga lineata AMNH APC 96-3 Furnarii Conopophagidae Conopophagidae Conopophaga aurita LSU B-4685 Furnarii Conopophagidae Conopophagidae Rhinocrypta lanceolata AMNHPRS 1152 Furnarii Rhinocryptidae Rhinocryptidae Scytalopus magellanicus LSU B-8348 Furnarii Rhinocryptidae Rhinocryptidae Pteroptochos castaneus AMNH RTC 471 Furnarii Rhinocryptidae Rhinocryptidae Melanopareia torquata LSU B-14572 Furnarii Rhinocryptidae Rhinocryptidae Smithornis rufolateralis AMNH MKW 448 Pitti Eurylaimidae Eurylaimidae Neodrepanis coruscans FMNH 8049 Pitti Philepittidae Philepittidae Pitta guajana AMNH PRS 732 Pitti Pittidae Pittidae Myzomela cardinalis AMNH MKL 33 Passeres Meliphagidae Meliphagidae Corvus brachyrhynchus AMNHPRS 1180 Passeres Corvidae Corvidae Sylvia runa AMNH LMC 95-13 Passeres Sylviidae Sylviidae Aimophila botterii UABC TRH 3572 Passeres Emberizidae Fringillidae Acanthisitta chloris ROM RIF002 incert. sedis Acanthisittidae Acanthisittidae Campethera nivosa AMNH PRS 2012 Piriformes Picidae Picidae Higher-level group names, except for Piriformes, were taken from Raikow (1987): the Tyranni and Furnarii are the two groups of New World suboscines, the Pitti are the Old World suboscines, and the Passeres are the oscine passerines. Family groupings prior to Sibley and Monroe (1990) are a composite of major sources. Abbreviations: Tyrann., Tyrannidae; Conopo., Conopophagidae; Piprid., Pipridae; Cot., Coting., Cotingidae; Phytotom., Phytotomidae; and Oxyrun., Oxyruncidae. 14 R.T. Chesser I Molecular Phylogenetics and Evolution 32 (2004) 11-24 from Prychitko and Moore (1997). Primers used for re- freq. [A] = 0.2883, freq. [C] = 0.1889, freq. [G] = amplifications, in addition to FIBI7U and FIBI7L, were 0.2095, freq. [T] = 0.3133; and shape parameter = FIBI7-397U (5'-AGTAACATATAATGGTTCCTGA 4.0335. For the mitochondrial data, the GTR-i-G + I A-3'), FIBI7-413U (3'-TCCTGAAGAAAGAGACAG model (General Time Reversible + Gamma + Proportion GTAGCAT-3'), FIBI7-439L (5'-CAACTGAGCTCC Invariant; Swofford et al., 1996) was most efficient and TGTCTTCTGAGTAGG-3'), and FIBI7-453L (5'-GTA the following settings were used: prob. [A-C] = 0.6009, CTTTACAACTGAGCTCCT-3'). Primers used for the prob. [A-G] = 14.2877, prob. [A-T] = 2.8370, prob. mitochondrial genes ND3 and COII were those detailed [C-G] = 0.7893, prob. [C-T] = 28.6713, prob. previously (Chesser, 1999, 2000). Sequencing was con- [[G-T]] = 1.0000; freq. [A] = 0.3750, freq. [C] = 0.3696, ducted using an ABI 377 automated sequencer (Applied freq. [G] = 0.0608, freq. [T] = 0.1946; shape parame- Biotechnologies). Mitochondrial sequences were aligned ter =0.4087; and proportion of invariant sites = 0.3639. using Sequencher 4.1 (GeneCodes Corp, 2000), and For the combined data, the GTR + G + I model was nuclear sequences were aligned using ClustalX 1.8 again most efficient and the following settings were used: (Thompson et al., 1997) with obvious errors corrected by prob. [A-C] = 0.7673, prob. [A-G] = 3.3216, prob. eye. Apparent heterozygosities were coded using the [A-T] = 1.0182, prob. [C-G] = 0.4112, prob. [C-T] = lUPAC ambiguity codes. All sequences used in this study 6.8899, prob. [[G-T]] = 1.0000; freq. [A] = 0.3354, freq. have been deposited in GenBank (Accession Nos. [C]= 0.3030, freq. [G] = 0.1368, freq. [T] = 0.2248; AY489408-AY489556). shape parameter = 0.4461; and prop, invar, sites = Data analysis was performed using the computer 0.0978. Character support for maximum likelihood programs PAUP* 4.0b8a (Swofford, 2001) and MacC- phylogenies was assessed via bootstrapping (Felsenstein, lade 4.0 (Maddison and Maddison, 2000). Data were 1985) using 100 heuristic pseudoreplicates with single analyzed using maximum parsimony and maximum random addition replicates. likelihood approaches, with C. nivosa designated the outgroup in all analyses. Parsimony analyses were conducted using heuristic searches, with equal character 3. Results weighting and 100 random addition replicates. Nuclear and mitochondrial data were analyzed separately and The aligned nuclear dataset consisted of 1013 char- combined (total evidence). Nucleotide gaps were treated acters; individual intron 7 sequences ranged in length as missing data, but nucleotide gaps of two or more from 831 to 897 bases. There were 746 variable charac- bases were subsequently mapped onto the nuclear and ters, 489 of which were potentially phylogenetically in- combined phylogenetic trees. Due to the relatively high formative. Uncorrected pairwise divergence ranged from levels of homoplasy and character saturation in the 1.0% between the two species of Conopophaga to 24.3% mitochondrial dataset, mitochondrial analyses were also between the woodpecker C. nivosa and S. aenigma. Un- conducted using various character weighting schemes, corrected pairwise divergence within New World su- including 2:1 transversion-transition weighting and boscines was as high as 14.8% (between Schiffornis downweighting of characters at third positions by fac- turdinus and Synallaxis cinerascens). The transition- tors of 2, 5, and 10. Character support for parsimony- transversion ratio for the dataset, calculated from the based phylogenies was assessed via bootstrapping most parsimonious trees, was 1.98, and average GC (Felsenstein, 1985), using 100 heuristic searches with 10 content of the sequences was 34.9%. The nuclear dataset random addition replicates each, and branch support contained 13 potentially phylogenetically informative (Bremer, 1988, 1994), which was computed using the insertion/deletion events of two or more base pairs. computer program TreeRot, version 2 (Sorensen, 1999). The ahgned mitochondrial dataset consisted of 1036 Maximum likelihood analyses were performed on the characters. Although the COII sequences contained no separate and combined data using heuristic searches indels, the ND3 sequence of C. nivosa contained a single with 10 random addition replicates. The program base insertion following position 173; this insertion is MODELTEST (Posada and Crandall, 1998) was used to typical of a variety of non-passerine taxa (Mindell et al., evaluate a variety of models of sequence evolution for 1998). Of the 1036 mitochondrial characters, 563 were maximum likelihood analysis. Using likelihood ratio variable and 495 potentially parsimony informative. tests, MODELTEST determines the model of sequence Uncorrected pairwise divergence ranged from 8.6% be- evolution that most efficiently maximizes likelihood, tween the two species of Conopophaga to 26.1% between while minimizing the number of model parameters. For the passerine Sylvia nana and the Old World suboscine the nuclear data, the HKY85 + G model (Hasegawa- Neodrepanis coruscans. Uncorrected pairwise divergence Kishino-Yano + Gamma; Hasegawa et al., 1985; Yang, within New World suboscines was as high as 21.5% 1994) was most efficient and the following settings, de- (between Tyranneutes stolzmanni and Melanopareia rived from MODELTEST, were used in the likelihood torquatus). The transition-transversion ratio for the analysis: TI/TV (transition/transversion) ratio = 2.027; dataset, calculated from the most parsimonious tree, R T. Chesser I Molecular Phylogenetics and Evolution 32 (2004) 11-24 15 was 2.36. Base composition was biased towards A, T, Ahlquist, 1990). The Broad-billed Sapayoa S. aenigma, and C (base frequencies of 27-31%), with average fre- resident of a narrow zone of rainforest from Panama to quency for G of only 13.2%. Ecuador, received strong support (100% bootstrap) as an Old World suboscine. 3.1. Phylogenetic analyses•nuclear Monophyly of New World suboscines, excluding S. aenigma, was strongly corroborated by the bootstrap Parsimony analysis of the nuclear data yielded 168 consensus tree (Fig. 2), with a bootstrap value of 96%. most parsimonious trees of 1932 steps (CI = 0.60, CI The primary split within suboscines resulted in a tyr- excluding uninformative characters = 0.51, RI = 0.64); annoid clade (Tyranni), consisting of all representatives mean number of changes per variable character on the of the Tyranninae, Tityrinae, Pipromorphinae, Cotin- most parsimonious trees was 2.6. The bootstrap con- ginae, and Piprinae; and a second clade consisting of sensus tree (Fig. 2) indicated that the New Zealand wren furnarioid taxa (Furnarii), including all representatives A. chloris, member of a group sometimes considered of the Furnariinae, Dendrocolaptinae, Thamnophilidae, suboscine, was sister to ah other passerines, consistent Formicariidae, Conopophagidae, and Rhinocryptidae with previous studies using sequence data (Barker et al., (usage of family/subfamily names following Sibley and 2002; Ericson et al., 2002). Within the remainder of the Ahlquist, 1990). These results also received strong passerines, the suboscines and oscines formed mono- bootstrap support (100 and 96%, respectively). phyletic groups. Two well-supported clades were also Within the Tyranni, the bootstrap tree (Fig. 2) revealed present within the suboscines; however, these differed three clades, which diverged in a polytomy. The first from the accepted biogeographic division between Old consisted of the Tyranninae and the Pipromorphinae, World and New World suboscines (Irestedt et al., 2001; which were monophyletic sister groups, and the single Raikow, 1987; Raikow and Bledsoe, 2000; Sibley and taxon O. cristatus, which was sister to these; the second

Campethera 78 r Sylvia 58 pr 100 Aimoptiila oscine passerines "ol Corvus 12 Myzomela Pitta 100 Sapayoa "Old World" suboscines 17 Smitliornis Neodrepanis Muscisaxicola El I 2 ' Tyrannus Tyranninae 75 4 I ElaeniaElaenia Hemitriccus Todirostrum Corythopis Pipromorphinae Mionectes Leptopogon Oxyruncus • sharpbill Tyranni Laniocera 78 Schiffornis lodopleura Tityrinae Tityra Pachyramphus Pipra J 10 ' Machaeropterus Piprinae ' TyranneutesTyn 3 1 Phytotoma \ 0 I Procnias Cotinginae 1 /Rupicola Drymornis Lepidocolaptes Dendrocolaptinae Dendrocincia Furnarius 96 Automolus Synallaxis Furnariinae Margaromis Sclerurus Ceositta Formicarius - - Formicariidae EPteroptochos Rhinocrypta Rhinocryptidae Scytalopus 1001IUU| Grallaricula kjiaifciiiowia ant-pittas Furnarii RJi Myrmothera [formerly Formicariidae] 1 Granaría 96 I Frederickena 100 Pyriglena Thamnophilidae 58 7 Myrmottierula I Pithy s lOOi Conopo. lineata Conopophagidae 25 ' Conopo. aurita Melanopareia • crescent-chests Acanthisitta • New Zealand wrens

Fig. 2. Phylogenetic relationships among suboscine birds based on maximum parsimony analyses of the nuclear sequence data. Trees shown are bootstrap consensus trees; numbers above branches are bootstrap values and numbers below are decay indices. 16 R T. Chesser I Molecular Phylogenetics and Evolution 32 (2004) 11-24 consisted of the Tityrinae {Schijfornis, Laniocera, lodo- the nuclear parsimony tree. Noteworthy differences be- pleura, Pachyramphus, and Tityrd) and Piprinae (includ- tween parsimony and likelihood trees involved the rela- ing Tyranneutes); and the third of the Cotinginae tionships of the sharpbill Oxyruncus, which was sister to (including Phytotomd). Within the Furnarii, three clades the Piprinae/Tityrinae in the likelihood analysis but sister also diverged in a polytomy. The first was a large clade to the Tyranninae/Pipromorphinae in the parsimony containing the Dendrocolaptinae/Furnariinae, a para- analysis, and relationships of the family Cotinginae, phyletic Formicariidae (sensu stricto), and most of the which was sister to the Tyranninae/Pipromorphinae in the Rhinocryptidae (excluding Melanopareia). Within this hkelihood analysis but was unresolved in the parsimony clade, Formicarius was sister to the dendrocolaptines/ analysis. However, as with the parsimony analysis, nei- furnariines. The Dendrocolaptinae, although monophy- ther likelihood result was strongly supported (bootstrap letic, grouped within the Furnariinae; the furnariines values <50%). Geositta and Sclerurus were sister to the rest of the Den- All major family and subfamily-level results found in drocolaptinae/Furnariinae. The rhinocryptids were sister the nuclear parsimony tree were also recovered in the to the dendrocolaptine/furnariine/i^oí-OT/cízrráí clade, and hkelihood analyses. However, bootstrap support (Fig. 3) the rest of the Formicariidae (Grallaria, Myrmothera, and for the likelihood results was generally higher than in the Grallaricula) was sister to this large grouping. The second parsimony analysis. For example, support for monophyly major clade within the Furnarii consisted of the Tham- of the Tyranninae/Pipromorphinae clade (87%), of the nophilidae and Conopophagidae, and the third consisted Piprinae/Tityrinae clade (84%o), of the Formicarius/Dsn- of the single taxon M. torquata. drocolaptinae/Furnariinae clade (65%), and of the Strong support was present for most subfamily and Thamnophilidae/Conopophagidae clade (78%) were all family groupings of Sibley and Ahlquist also identified noticeably higher than in the parsimony tree, as was here as clades; bootstrap values ranged from 88% for support for monophyly of suboscines as a group (97%). Pipromorphinae to 100% for Piprinae, Thamnophilidae, and Conopophagidae, with the exception of 73% for the 3.2. Phylogenetic analyses•mitochondrial and combined modified Tityrinae and 52%o for the modified Rhino- cryptidae (Fig. 2). Support for relationships among these Parsimony analysis of the mitochondrial data, using groups was lower and, with the exception of 99%) sup- equal weighting of characters, resulted in two most par- port for the clade uniting the Dendrocolaptinae with a simonious trees (not shown) of 5133 steps (CI = 0.19, CI paraphyletic Furnariinae, ranged from <50% for any excluding uninformative characters = 0.18, RI = 0.32); sister group relationship involving the Cotinginae or mean number of changes per variable character on the M. torquatus, to 74%) for a sister group relationship be- most parsimonious mitochondrial tree was 9.1. Despite tween the Tyranninae and the Pipromorphinae (Fig. 2). extremely high levels of homoplasy in this dataset, the Mapping of insertion/deletion events onto the nuclear most parsimonious trees under the various weighting re- consensus tree revealed that one indel was a synapo- gimes shared a number of features with the nuclear trees, morphy for all suboscines and three others were syna- including monophyly of New World suboscines (exclud- pomorphies uniting S. aenigma with the Old World ing S. aenigma), monophyly of the Tyranninae/Pipro- suboscines. Indels also supported the monophyly of the morphinae clade, monophyly of the Tityrinae/Piprinae Tyranni, the Tityrinae, and the Rhinocryptidae (ex- clade, monophyly of the Cotinginae, Piprinae, Dendro- cluding Melanopareia). Other indels occurred only colaptinae, and Conopophagidae, polyphyly of the tra- among specific taxa within the Pipromorphinae, the ditional Formicariidae, and paraphyly of the traditional Cotinginae, the Dendrocolaptinae/Furnariinae, and the Furnariidae. As in the nuclear trees, Geositta and Formicariidae. A partially homoplasious indel was Sclerurus were sister to a clade consisting of the other found in the oscine passerines, two dendrocolaptines dendrocolaptines and furnariines. The bootstrap con- {Lepidocolaptes and Drymornis) and one rhinocryptid sensus trees of the mitochondrial data were largely unre- {Pteroptochos), and another occurred only in two tity- solved, although monophyly of the Tyranninae, rines {Schijfornis and Laniocera), one furnariine {Fur- Dendrocolaptinae, Thamnophilidae, and Conopophagi- narius), and one rhinocryptid (Rhinocrypta). dae received strong support. Results of the nuclear maximum likelihood analysis The combined nuclear and mitochondrial parsimony (Fig. 3) revealed two most likely trees (score-Ln = analysis resulted in three most parsimonious trees (not 11451.343) and supported all major findings of the par- shown) of 7113 steps (CI = 0.30, CI excluding uninfor- simony analyses, including the New Zealand wren as mative characters = 0.26, RI = 0.40); mean number of sister to all other passerines (although with weak sup- changes per variable character on the combined trees was port), monophyly of the Sapayoa-Old World suboscine 5.4. The combined bootstrap consensus tree was entirely clade, monophyly of the New World suboscines if Sapa- consistent with the nuclear bootstrap tree, although res- yoa is excluded, and monophyly of the Tyranni (excluding olution at medium depths was reduced. There was strong Sapayoa) and the Furnarii, and was virtually identical to support for monophyly of New World suboscines. R. T. Chesser I Molecular Phylogenetics and Evolution 32 (2004) 11-24 17

• Campethera 82 r • Sylvia eirn. Aimoptiila 100 Corvus - Myzomela Pitta 100 Smittiornis Neodrepanis Sapayoa Tyrannus Muscisaxicola Elaenia Hemitriccus Todirostrum Coryttiopis Mionectes Leptopogon Ptiytotoma Procnias

97 Laniocera Sciiiffornis lodopleura Tityra Pachyrampiius Pipra Macliaeropterus Tyranneutes Oxyruncus 100 I Drymornis 91 -£r Lepidocolaptes 95 Dendrocincla 95r - Furnarius 99 Automolus 78 99 • Synallaxis • Margarornis 65 • Sclerurus Geositta 62 Formicarius Pteroptoctios 66 89 Rtiinocrypta Scytalopus 100 Grallaricula 99 Myrmothera Granaría 100 j Fredencl(ena 100 ' Pynglena j Myrmotherula 78 ' Pittiys 100 J• Conopo. lineata "T- Conopo. aurila Melanopareia Acanthisitta 0.01 substitutions/site

Fig. 3. Phylogram showing relationships among suboscine birds based on maximum likelihood analysis of sequence data from intron 7 of the nuclear gene ß-fibrinogen. Tyranni, and Furnarii (bootstrap support from 86 to very similar to the likelihood tree based on the nuclear 99%), and for all major family and subfamily groupings data (Fig. 3). Distinctive features of the combined like- except Tityrinae. Indeed, the combined results revealed lihood tree were the position of the Cotinginae as sister improved support for several family/subfamily groups to the remainder of the Tyranni and the position of (Tyranninae, Dendrocolaptinae, and Rhinocryptidae), Melanopareia as sister to the Thamnophilidae/Conop- but relationships among family/subfamily groups were ophagidae clade within the Furnarii. largely unresolved, especially within the Furnarii. Like- wise, the positions of Oxyruncus and Melanopareia within the Tyranni and Furnarii, respectively, were unresolved. 4. Discussion Likelihood analysis of the mitochondrial data revealed a most likely tree (score -Ln = 19691.279; not 4.1. Higher-level systematics shown) virtually identical to the mitochondrial parsimony tree, containing all major features described for This study indicates polyphyly of New World subos- the most parsimonious mitochondrial tree. cines and possible paraphyly of Old World suboscines, Likelihood analysis of the combined tree yielded a due to the phylogenetic position of the appropriately most likely tree (score •Ln = 32377.321; not shown) named S. aenigma. The affinities of this species with Old R T. Chesser I Molecular Phylogenetics and Evolution 32 (2004) 11-24

World suboscines mean that suboscines resident in the certain aifinities within the group (Table 1). These have New World constitute two distinct lineages, one appar- included the genera Oxyruncus, Phytotoma, Corythopis, ently consisting of a single species, the other apparently Schijfornis, Tityra, Pachyramphus, lodopleura, Lanio- made up of the remaining 1000+ species of New World cera, and Tyranneutes, among others. Based on mor- suboscines. Whether Sapayoa was always the only New phological data, O. cristatus has been alternately placed World representative of the "Old World" suboscine in its own family (e.g., Ames, 1971; Traylor, 1979; lineage, or whether it is the sole surviving species from a Wetmore, 1960) or merged into the Tyrannidae (Mayr New World radiation of this lineage, is unknown; never- and Amadon, 1951). More recently, the molecular data theless, this remarkable result provides the only known of Sibley et al. (1984), Sibley and Ahlquist (1985, 1990), instance of pantropical distribution among the large and Prum et al. (2000) placed Oxyruncus well within the avian order Passeriformes, and in fact echoes results from Cotingidae. The genus Phytotoma was traditionally other research. Lanyon (1985), for example, in an elec- placed in its own family, although much recent evidence trophoretic study of the Tyrannoidea, found Sapayoa to (Johansson et al., 2002; Lanyon, 1985; Lanyon and be only distantly related to the other taxa studied, and Lanyon, 1989; Prum et al., 2000; Sibley and Ahlquist, suggested that its true affinities may be outside the tyr- 1990) indicates that the plantcutters are cotingas. annoids. Likewise, Sibley and Ahlquist (1990) included Corythopis torquatus was traditionally included in the Sapayoa in their DNA-DNA hybridization studies, Conopophagidae (in the Furnarii), but more recently where their melting curves indicated its possible rela- has been consistently placed in the Tyrannidae (Ames, tionship with Old World suboscines. However, they were 1971; Ames et al., 1968; Meyer de Schauensee, 1970; evidently uncertain of these data and excluded Sapayoa Sibley and Ahlquist, 1985, 1990; Traylor, 1977, 1979; from their phylogenetic analyses. but see Johansson et al., 2002). S. turdinus generally has With the exception of S. aenigma, the data presented been proposed as a member of the Pipridae, but has also above corroborate the monophyly of New World subos- been considered part of the Cotingidae (Wetmore, 1972) cines and support the basic biogeographical dichotomy or Tyrannidae (Ames, 1971), or even as evidence that between New World and Old World suboscines. Tradi- the "traditional division of the manakin-cotinga-fly- tional classifications, such as those of Mayr and Amadon catcher complex into three families cannot be main- (1951) and Wetmore (1960), had placed most suboscines, tained" (Snow, 1973). Sibley and Ahlquist included including the Old World pittas, asities, and New Zealand Schijfornis in their Tityrinae, whereas Prum and Lanyon wrens (then considered suboscines) and all the New (1989) included it in their eponymous Schijfornis group. World taxa, in a suborder separate from that of the Old Traditional morphological studies have placed the gen- World broadbills (Eurylaimi), and included the pittas and era Tityra, Pachyramphus, lodopleura, and Laniocera asities with the New World tyrannids, cotingas, plant- alternately in the Cotingidae or the Tyrannidae (sum- cutters, manakins, and sharpbill in the superfamily Tyr- marized in Prum and Lanyon, 1989). Sibley and Ahl- annoidea. Suggested rearrangements such as that of quist (1985, 1990) placed Tityra and Pachyramphus in Olson (1971) also involved an admixture of Old World their subfamily Tityrinae; their studies did not include and New World groups, although Ames (1971) suggested lodopleura or Laniocera, but Sibley and Monroe (1990) that the suborder Tyranni, previously consisting of all placed these genera in the Cotinginae and Tyranninae, suboscines other than the Eurylaimi, be restricted to the respectively. Pachyramphus, lodopleura, and Laniocera New World members of the superfamily Tyrannoidea formed part of the Schijfornis group of Prum and (Tyrannidae, Cotingidae, Phytotomidae, Pipridae, and Lanyon (1989), but Tityra was specifically excluded Oxyruncidae). The modern view of the basic biogeo- from this group. The genus Tyranneutes has been typi- graphical division between Old World and New World cally placed in the family Pipridae, although Prum suboscines, enunciated by Sibley and Ahlquist (1985, (1990a) determined that it was not a manakin, but one 1990; Fig. 1) and Raikow (1987), is strongly supported by of a group of non-piprid tyrannoids erroneously placed the DNA sequence data presented above (again, with the in the family. exception of Sapayoa). Likewise, the sequence data sup- Relationships within tyrannoid groups, especially port the division of New World suboscines into a tyran- within the traditional family Tyrannidae, have also been nid-related clade and a furnariid-related clade. This was a subject of controversy. Traylor (1977, 1979) used also the traditional view, except that the Old World pittas, cranial (Wärter, 1965) and other morphological, be- asities, and New Zealand wrens, as stated above, were havioral, and ecological data to extensively revise the typically included in the tyrannid-related clade. classification of the family, and recognized three core groups: Elaeniinae, Fluvicolinae, and Tyranninae. 4.2. Tyranni Traylor (1979) also tentatively included the genera Ti- tyra and Pachyramphus with the tyrannids, but pri- The tyrannoid suboscines have long been a confusing marily as taxa not easily placed elsewhere. Sibley and group, due in large part to the variety of taxa of un- Ahlquist (1985, 1990) and Sibley and Monroe (1990), in R. T. Chesser I Molecular Phylogenetics and Evolution 32 (2004) 11-24 19 contrast, split Traylor's core Tyrannidae into two quite quence data recognize the Tyranninae and Pipromor- different groups: Tyranninae, which included all the phinae as sister groups, as did the results of Johansson Tyranninae and Fluvicolinae and part of the Elaeniinae et al. (2002), supporting monophyly of Traylor's (1977, of Traylor (1977, 1979), and thus constituted the bulk of 1979) core group of tyrant-flycatchers. This arrange- the family; and Pipromorphinae (called Mionectidae in ment was also present in an alternate FITCH tree 1985), which consisted of the other genera in Traylor's (Fig. 4) presented by Sibley and Ahlquist (1990, their Elaeniinae, including MionectesIPipromorpha, Leptopo- Fig. 345). The Tityrinae were distant from these groups gon, Pseudotriccus, Poecilotriccus, Taeniotriccus, Hemi- and were the sister group to the manakins (Piprinae), a triccuslIdioptilon, Todirostrum, and Corythopis (Sibley clade that included Tyranneutes as sister to the "true and Ahlquist, 1990; Sibley and Monroe, 1990). Most manakins" Pipra and Machaeropterus, as in Lanyon surprisingly, the Tyranninae and Pipromorphinae were (1985). The sister relationship between tityrines and not sister groups in Sibley and Ahlquist's (1985, 1990) manakins was also partially consistent with Lanyon's phylogeny; rather, the Pipromorphinae were sister to all (1985) electrophoretic results. other tyrannoid groups (Cotinginae, Piprinae, Tityrinae, Consistent with the difficulties morphologists have Tyranninae). Thus, Sibley and Ahlquist found the tra- encountered in their attempts to classify it, the position ditional family Tyrannidae to be polyphyletic. of the sharpbill O. cristatus within the Tyranni was not The DNA sequence data clearly support the inclusion well resolved (see also Johansson et al., 2002). In anal- of Phytotoma in the Cotinginae and Hemitriccus, Tod- yses of the sequence data, Oxyruncus appears variously irostrum, Corythopis, Mionectes, and Leptopogon in the as sister to the Tyranninae/Pipromophinae, sister to the Pipromorphinae. While these results are congruent with Piprinae/Tityrinae, or sister to the Cotinginae. This re- those of Sibley and Ahlquist (1985, 1990) and Johansson sult contrasts markedly with those of Sibley and Ahl- et al. (2002), the pipromorphine results contrast with a quist (1985, 1990) and Prum et al. (2000), who variety of previous studies of tyrant-flycatchers. concluded that Oxyruncus is nested deep within the Monophyly of the Pipromorphinae, for example, was cotingas. However, the cytochrome b sequence used by supported by neither protein electrophoresis (Lanyon, Prum et al. (2000) was recently proposed to have been 1985) nor syringeal morphology (Lanyon, 1988a,b), nor erroneous (Johansson et al., 2002). Furthermore, the does such a group appear in traditional classifications, electrophoretic study of Lanyon (1985), despite exten- although Wolters (1977; after Bonaparte, 1853), used sive sampling of cotingas, also failed to place Oxyruncus the same name to refer to a subfamily consisting solely in the Cotinginae; rather, it appeared to be more closely of the genera Mionectes and Pipromorpha. related to members of the Tyranninae or Tityrinae. The sequence data also support a monophyletic Ti- tyrinae; however, this group consists of an amalgama- tion of the Schiffornis group (Prum and Lanyon, 1989) Oxyruncus with Sibley's Tityrinae (cf. Johansson et al., 2002). The Schiffornis group consisted of the six genera Schiffornis, Cotinginae Laniisoma, lodopleura, Laniocera, Xenopsaris, and Tityrinae Pachyramphus. Sibley and Ahlquist, as noted above, restricted their Tityrinae to Tityra, Pachyramphus, and Piprinae Schiffornis. The sequence data identified Schiffornis, Tyranninae Laniocera, lodopleura, Pachyramphus, and Tityra as a Pipromorphinae reasonably well-supported clade, with strong support for internal groupings of Laniocera and Schiffornis, and Fumariidae Tityra, Pachyramphus, and lodopleura, respectively. Formicariidae Laniisoma and Xenopsaris were not sequenced for this study, although the mitochondrial data of Prum et al. Rhinocryptidae (2000) supported inclusion of Laniisoma in a group containing Schiffornis, lodopleura, Pachyramphus, and ant-pittas Tityra. Despite the suggestion of Prum et al. (2000) that - Conopophagidae • both the Schiffornis group and Sibley's Tityrinae may be valid higher-level taxa, both groups are demonstrably - Ttiamnophilidae - paraphyletic in the phylogenetic trees presented above. Fig. 4. Evolutionary relationships among major groupings of subos- Although the Tyranninae, Tityrinae (as modified cine birds. Phylogeny on the left side is based on an alternate (FITCH) above), and Pipromorphinae all form well-supported analysis of the DNA-DNA hybridization data of Sibley and Ahlquist (1990, their Fig. 345). Phylogeny on the right is simplified from the clades in the analyses presented here, relationships DNA sequence results presented above. Note that Oxyruncus cristatus among these groups differed considerably from those (the Sharpbill) is included within the Cotinginae and that the antpittas presented by Sibley and Ahlquist (1985, 1990). The se- are included in the Formicariidae in Sibley and Ahlquist's tree. 20 R T. Chesser I Molecular Phylogenetics and Evolution 32 (2004) 11-24

4.3. Furnarii drocolaptids. Interestingly, Ames (1971) concluded that Geositta was the only furnariid genus to possess horns in The furnarioids have historically been characterized the syrinx, a trait he found in all dendrocolaptids, sug- by relatively well-defined families with few problemati- gesting that Geositta is a morphologically atypical fur- cal taxa, but relationships among families have re- nariid genus. Ames examined the species Geositta mained obscure. Relationships within the large cunicularia in his study, the same species sequenced here. traditional families Furnariidae and Formicariidae have These findings contrast markedly with the DNA hy- likewise been subject to debate. There has long been bridization results of Sibley and Ahlquist (1985, 1990), discussion, for example, of whether the Dendrocolapti- who found Geositta to nest deep within the Furnariidae. dae are separable as a family from the closely related It is unclear which species of Geositta was included in Furnariidae (summarized in Feduccia, 1973). This dis- Sibley's hybridization experiments, however, and it is cussion has typically focused on the degree of morpho- possible that this discrepancy is due to sampling differ- logical difference between the two groups, rather than ent branches of a polyphyletic genus. questions of monophyly. However, Feduccia's "hypo- The data presented here also support the separation thetical phylogeny" (Fig. 20 in Feduccia, 1973) clearly of the "ground antbirds" and "typical antbirds" or illustrates a paraphyletic Furnariidae if dendrocolaptids Formicariidae and Thamnophilidae (Sibley and Ahl- are excluded from the family (the synallaxine furnariids quist, 1985, 1990), as well as the paraphyly of the are sister to the remaining furnariids and dendrocol- ground antbirds (Formicariidae sensu stricto). The aptids), and Ihering (1915) proposed an apparently pa- antthrush Formicarius was not sister to the antpittas raphyletic Furnariidae, with woodcreepers having twice Grallaria, Myrmothera, and Grallaricula, consistent with arisen from within the Philydorinae. Although the other sequencing results (Irestedt et al., 2002; Rice, Formicariidae traditionally was considered a cohesive 2000). Furthermore, a sister relationship between the family, Ames (1971) found two distinct syringeal forms Thamnophilidae and the remainder of the Furnarii, as within the family, one in the "ground antbirds" and the proposed by Sibley and Ahlquist (1985, 1990), is in- other in the "typical antbirds," a division presaged by consistent with the sequence results above (see also Heimerdinger and Ames' (1967) study of sternal notches Irestedt et al., 2002), in which the Thamnophilidae are of suboscines. sister to the Conopophagidae; this clade is then sister to The DNA hybridization data (Sibley and Ahlquist, the remainder of the Furnarii (Fig. 4). 1985, 1990; Figs. 1 and 4) showed that although the Finally, the sequence data were unable to resolve the Furnariinae and Dendrocolaptinae were monophyletic position of the genus Melanopareia. Melanopareia has sister groups, the ground antbirds and typical antbirds generally been considered part of the furnarioid family were not: the typical antbirds (Thamnophilidae) were Rhinocryptidae, although Ridgely and Tudor (1994) the sister group to rest of the Furnarii, and placed in suggested that it is not rhinocryptid. The genus was not Sibley and Ahlquist's classification into a distinct parv- included in the studies of Sibley and Ahlquist (1985, order, whereas the ground antbirds (Formicariidae) 1990). The trees of Irestedt et al. (2002) placed it in a were sister to a clade consisting of the Rhinocryptidae polytomy that also included the Thamnophilidae and and the Conopophagidae. This three-family clade was in the Conopophagidae, or as sister to the rest of the turn sister to the Furnariinae/Dendrocolaptinae clade. Furnarii, although support for these results was weak. The DNA sequence data of Irestedt et al. (2002) in- The sequence data presented here clearly place Mela- dicated that the traditional family Furnariidae is para- nopareia in the Furnarii, but it appears to be distantly phyletic if the dendrocolaptids are excluded; Sclerurus related to other furnarioids and its affinities within the was found to be sister to the remainder of the furnariid/ group remain uncertain. dendrocolaptid clade. Sibley and Ahlquist had previously shown that Sclerurus is a genetically atypical fur- 4.4. Comparing relationships among groups with results of nariid genus, but in their phylogeny it was sister to all the DNA hybridization studies other furnariids rather than to a furnariid/dendrocolaptid clade. Irestedt et al. (2002) also found the tradi- Although family and subfamily groups identified as tional family Formicariidae to be paraphyletic and monophyletic generally received strong support in the Sibley and Ahlquist's restricted Formicariidae to be analyses presented here, relationships among groups paraphyletic, as well, with the antpittas separated from were typically less well supported, and in some cases the antthrushes (see also Rice, 2000). were unresolved (Figs. 2 and 3). The sequence data presented here also show the Comparison of relationships among families and Furnariidae to be paraphyletic if the dendrocolaptids subfamilies in the DNA sequence results with those of are excluded. However, these data indicate that the ge- Sibley and Ahlquist (Figs. 1 and 4) revealed little con- nus Geositta, in addition to Sclerurus, lies outside the gruence. The proposed sister relationship between the clade consisting of the rest of the furnariids and den- Pipromorphinae and the rest of the tyrannoids (Sibley R. T. Chesser I Molecular Phylogenetics and Evolution 32 (2004) 11-24 21 and Ahlquist, 1990) was contradicted by the sequence presented here may bear directly on previous work data, as was the proposed sister relationship between the concerning the evolution of morphology, ecology, or Thamnophilidae and the rest of the furnarioids. Indeed, behavior, despite the focus of this study on higher-level no sister group relationship within the tyrannoids or the relationships and the necessarily limited intrafamilial furnarioids was present in both the preferred (UPGMA) sampling. phylogeny of Sibley and Ahlquist (Fig. 1) and the DNA Syringeal characters have played a prominent role in sequence trees presented above. suboscine systematics as far back as the landmark works Critics have noted that many internal branches in of Müller (1847) and Garrod (1876). A key character Sibley and Ahlquist's (1985, 1990) phylogeny are un- within the tyrannoids has been the presence of internal stable and not robust to different types of analysis syringeal cartilages, proposed by Ames (1971) as a syn- (e.g., Cracraft, 1987; Harshman, 1994; Lanyon, 1985). apomorphy for the tyrant-flycatchers (traditional family For example, the alternate FITCH tree (Fig. 4, left), Tyrannidae). However, several other tyrannoids were presented but only briefly discussed by Sibley and discovered to share this character (Lanyon, 1984; Prum, Ahlquist (1990, their Fig. 345), depicted several rela- 1990a; Prum and Lanyon, 1989), and the homology of tionships not present in their preferred phylogeny many of these structures has been questioned (Prum, (their UPGMA tree), especially among the tyrannoids. 1990a; Prum and Lanyon, 1989). Sibley and Ahlquist's Noteworthy among these was a sister relationship hypothesis that the traditional family Tyrannidae is between the Tyranninae and the Pipromorphinae, as polyphyletic, and that part of the tyrannids form a sister reported in this study and in Johansson et al. (2002), group to a clade consisting of the cotingas, manakins, supporting monophyly of the tyrant-flycatchers if the tityrines, and remaining tyrant-flycatchers, suggested tityrines are excluded. Also notable was the absence of that internal syringeal cartilages evolved independently a sister group relationship between the Piprinae and in the pipromorphines and the tyrannines and were not the Cotinginae, a result that contradicts most tradi- homologous. This hypothesis was met with skepticism by tional views but is consistent with the sequence results at least one syringeal morphologist (Lanyon, 1988a). The presented above. sequence data presented above support monophyly of a Harshman (1994) re-analyzed the data of Sibley and tyrannine/pipromorphine clade relative to tyrannoids Ahlquist (1990), introducing random ordering of taxa, that lack internal syringeal cartilages (most Piprinae and the use of additional tree-building algorithms, and sin- Cotinginae) and other tyrannoids that possess these gle-taxon jackknifing procedures, then constructed a cartilages, including the tityrines, Oxyruncus, Tyranne- jackknife consensus tree of all the best-fit trees. Al- utes and several other piprid-like taxa, and the cotingid though 56% of the interior branches included in Sibley genus Lipaugus (McKitrick, 1985; Prum, 1990a; Prum and Ahlquist (1990)'s FITCH trees remained intact in and Lanyon, 1989). Thus, at a minimum, homology of re-analyses of their data for all birds, interior branches the internal cartilages of the Tyranninae and the Pipro- within the tyrannoid and furnarioid New World su- morphinae is supported by the sequence data. Internal boscines became near-complete polytomies (Harshman, syringeal cartilages among a wider group of tyrannoids 1994). Within the Tyranni, the Tyranninae, Piprinae, may also be homologous, depending on resolution of the Cotinginae, Tityrinae, and Pipromorphinae all collapsed polytomies within the Tyranni. into a polytomy; and within the Furnarii, the Tham- Nest placement and nest structure in the traditional nophilidae were sister to a polytomy consisting of the Furnariidae are among the most diverse of any bird Dendrocolaptinae, the Furnariinae, the Conopophagi- family, and the evolution of nest-building in this group dae, the Rhinocryptidae, and the Formicariidae. Even is of great behavioral interest. Zyskowski and Prum this single internal branch, as noted above, is not sup- (1999) recently provided a phylogenetic analysis of the ported by the DNA sequence results. furnariines based on careful examination of nests and nesting behavior. They concluded that "comparisons 4.5. Implications for character evolution with outgroups demonstrate that cavity nesting is ple- siomorphic to the family," based on the phylogeny of Suboscines are the most species-rich constituent of Sibley and Ahlquist, in which the Dendrocolaptidae and the world's most species-rich avifauna, that of the their Formicaroidea (Formicariidae, Conopophagidae, Neotropics, and their morphological, behavioral, and and Rhinocryptidae) were successive outgroups to the ecological diversity is equally impressive. Studies of be- Furnariidae. Although cavity nesting is characteristic of havioral evolution in particular families have been es- the dendrocolaptids, it is only one of several nesting types pecially prominent (e.g., Fitzpatrick, 1985; Prum, 1990b, found in the Formicaroidea and the Furnariidae, and it 1994; Skutch, 1996; Snow, 1976; Zyskowski and Prum, seems unclear without detailed within-group phyloge- 1999), due to the variety of mating systems, displays, netic analysis whether cavity nesting is actually the an- nest types, foraging behavior, diet, and other characters cestral form of furnariid nest. The DNA sequence data, exhibited by suboscine birds. The DNA sequence results however, despite the merging of the Dendrocolaptinae 22 R T. Chesser I Molecular Phylogenetics and Evolution 32 (2004) 11-24 into the Furnariinae, considerably strengtiien the case Porini, Secretaria de Recursos Naturales y Ambiente that cavity nesting is the ancestral state of furnariids. Humano, Buenos Aires, Argentina; and Juan Carlos Formicarius and other antthrushes, sister to the furnariid Cuchacovich, Servicio Agrícola y Ganadero, Santi- clade (consisting of all furnariines and dendrocolap- ago, Chile, kindly granted collecting and export per- tines), are obligate cavity nesters. Within the Furnarii- mits for their respective jurisdictions. I thank George dae, Geositta and Sclerurus, sisters to the rest of the Barrowclough and Paul Sweet for providing tissue group, are both obligate cavity nesting genera. The from the Department of Ornithology, American remainder of the group consists of two clades, one of Museum of Natural History; Fred Sheldon and which (the dendrocolaptines) is an obligate cavity nest- Donna Dittmann for providing tissue from the Ge- ing group, the other of which (the rest of the furnariines) netic Resources Collection, Louisiana State University contains cavity nesting along with a variety of other Museum of Natural Science; Shannon Hackett and nesting types. Thus, under the first doublet rule Dave Willard for providing tissue from the Bird (Maddison et al., 1984), the unequivocal most parsi- Division, Field Museum of Natural History; Tom monious character state of the ancestors both of the Huels for providing tissue from the University of Furnariidae as a whole and of the Furnariidae excluding Arizona Bird Collection; Gary Voelker for providing Geositta and Sclerurus, is cavity nesting. tissue from the Marjorie Barrick Museum, University The evolution of other behavioral characters likely of Nevada Las Vegas; and Allan Baker for providing bears re-evaluation in light of the phylogenetic data tissue from the Royal Ontario Museum. I thank presented above. For example, the evolution of mating Keith Barker and Rob Moyle for sequencing several systems and display behavior among manakins (Pipri- difficult pieces of DNA, and Julie Feinstein and Jeff nae) and other tyrannoids has been traditionally inter- Groth for laboratory assistance and advice. This preted in the context of a sister group relationship study was funded in part by the Frank M. Chapman between the manakins and the cotingas. However, the Memorial Fund of the American Museum of Natural DNA sequence data indicate that the Piprinae are the History. The research reported in this paper is a sister group to the Tityrinae. Prum and Lanyon (1989), contribution from the Lewis B. and Dorothy Cull- in their discussion of the Schijfornis group, suggested man Research Facility at The American Museum of that Schijfornis and Laniocera may be dispersed lekking Natural History and has received generous support genera and that Pachyramphus and lodopleura are mo- from the Lewis B. and Dorothy CuUman Program nogamous genera. They indicated that the sister group for Molecular Systematic Studies, a joint initiative of of the Schijfornis group was unknown, but suggested The New York Botanical Garden and The American that these species are probably not closely related to the Museum of Natural History. true lekking lineages of the Tyranni, and that monog- amy was the likely ancestral breeding system in the group. A sister group relationship between the Piprinae References and the Tityrinae suggests that the lekking behavior exhibited by such genera as Schijfornis may not repre- Ames, P.L., 1971. The morphology of the syrinx in passerine birds. sent an independent development to that in the Piprinae. Bull. Peabody Mus. Nat. Hist. 37, 1-194. Although the ancestral character state cannot be thor- Ames, P.L., Heimerdinger, M.A., Warter, S.L., 1968. The anatomy and systematic position of the antpipits Conopophaga and Cory- oughly evaluated without a much more complete thopis. Postilla 114, 1-32. phylogeny, it appears at the very least that the evolution Barker, F.K., Barrowclough, G.F., Groth, J.G., 2002. A phylogenetic of breeding systems within the Tityrinae/Piprinae, and hypothesis for passerine birds: taxonomic and biogeographic perhaps elsewhere within the Tyranni, should be re- implications of an analysis of nuclear DNA sequence data. Proc. examined. R. Soc. Lond. B 269, 295-308. Bonaparte, C.L., 1853. Classification ornithologique par séries. C. R. Acad. Sei. Paris 37, 641-647. Bremer, K., 1988. 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